The predictable occurrence of whale sharks, Rhincodon typus, has been well documented in several areas. However, information relating to their migratory patterns, residency times and connectivity across broad spatial scales is limited. In the present study photo-identification data is used to describe whale shark population structure and connectivity among known aggregation sites within the Western Central Atlantic Ocean (WCA). From 1999 to 2015, 1,361 individuals were identified from four distinct areas: the Yucatan Peninsula, Mexico (n = 1,115); Honduras (n = 146); northern Gulf of Mexico, United States (n = 112), and Belize (n = 49). Seasonal patterns in whale shark occurrence were evident with encounters occurring in the western Caribbean Sea earlier in the year than in the GOM. There was also a significant sex bias with 2.6 times more males present than females. Seventy sharks were observed in more than one area and the highest degree of connectivity occurred among three aggregation sites along the Mesoamerican Reef. Despite this, the majority of resightings occurred in the area where the respective sharks were first identified. This was true for the WCA as a whole, with the exception of Belize. Site fidelity was highest in Mexico. Maximum likelihood modelling resulted in a population estimate of 2,167 (95% c.i. 1585.21-2909.86) sharks throughout the entire region. This study is the first attempt to provide a broad, regional population estimate using photo-identification data from multiple whale shark aggregations. Our aim is to provide population metrics, along with the description of region-scale connectivity, that will help guide conservation action in the WCA. At a global level, rapidly growing photographic databases are allowing for researchers to look beyond the description of single aggregation sites and into the ocean-scale ecology of this pelagic species.